CHAPTER 4-8 INVERTEBRATES: MOLLUSCSInvertebrates: Molluscs. Chapt. 4-8. In: Glime, J. M. Bryophyte Ecology. Volume 2. Bryological Interaction. 4-8-1 Ebook sponsored by Michigan Technological

Glime, J. M. 2017. Invertebrates: Molluscs. Chapt. 4-8. In: Glime, J. M. Bryophyte Ecology. Volume 2. Bryological Interaction. 4-8-1 Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Last updated 26 September 2017 and available at <http://digitalcommons.mtu.edu/bryophyte-ecology2/>.

CHAPTER 4-8 INVERTEBRATES: MOLLUSCS

TABLE OF CONTENTS Gastropoda: Snails and Slugs............................................................................................................................. 4-8-2 Reproduction................................................................................................................................................ 4-8-3 Mating and the Love Dart ..................................................................................................................... 4-8-4 Egg and Larval Development ............................................................................................................... 4-8-5 Bryophyte Interactions................................................................................................................................. 4-8-6 Abundance ................................................................................................................................................... 4-8-6 Adaptations .................................................................................................................................................. 4-8-7 Confusing the Predator ......................................................................................................................... 4-8-7 Jumping to Escape ................................................................................................................................ 4-8-7 Keeping It Small ................................................................................................................................... 4-8-8 Conical Shape ....................................................................................................................................... 4-8-9 Avoiding Desiccation............................................................................................................................ 4-8-9 No Shell – Slugs ................................................................................................................................. 4-8-10 In Search of Food....................................................................................................................................... 4-8-11 Low Palatability? ................................................................................................................................ 4-8-12 Low Nutritional Quality? .................................................................................................................... 4-8-14 Food for Some .................................................................................................................................... 4-8-14 An Avoidance of Gametophores? ....................................................................................................... 4-8-16 Deterrents to Herbivory ...................................................................................................................... 4-8-20 Digestibility ........................................................................................................................................ 4-8-21 Role in Bryophyte Competition with Lichens .................................................................................... 4-8-21 Palatable Gametophytes...................................................................................................................... 4-8-21 Aquatic Grazing.................................................................................................................................. 4-8-21 Bryophyte Antifeedants ............................................................................................................................. 4-8-22 Dispersal Agents ........................................................................................................................................ 4-8-23 Bryophytes as Home .................................................................................................................................. 4-8-28 Epiphytic............................................................................................................................................. 4-8-32 Calcareous Areas ................................................................................................................................ 4-8-33 Bogs and Mires ................................................................................................................................... 4-8-35 Aquatic................................................................................................................................................ 4-8-37 Plant Protectors .......................................................................................................................................... 4-8-38 Mussels (Bivalve Molluscs) .............................................................................................................................. 4-8-38 ECHINODERMATA........................................................................................................................................ 4-8-38 Summary ........................................................................................................................................................... 4-8-39 Acknowledgments............................................................................................................................................. 4-8-39 Literature Cited ................................................................................................................................................. 4-8-39

4-8-2 Chapter 4-8: Invertebrates: Molluscs

CHAPTER 4-8 INVERTEBRATES: MOLLUSCS

Figure 1. Slug on a Fissidens species. Is it eating, or just a casual visitor? Photo by Janice Glime.

The most familiar of the bryophyte inhabitants among the molluscs are the snails and slugs, but you will see that some bivalves also have an interesting relationship with bryophytes.

Mollusca are considered to be bilaterally symmetrical (like humans) (Pratt 1935), but they seem to push the definition to the limit. In bivalves, that is not too difficult to understand, but in snails the twisted body and shell seem to twist the definition as well; even organs normally paired, like kidneys, are not paired (Figure 2).

Gastropoda: Snails and Slugs Most terrestrial and freshwater snails (Pulmonata)

have spiral shells and these may be taller than the diameter of the opening (elongate/conical; Figure 26) or shorter (Figure 145) (Pratt 1935). The inside body is also a spiral, but it is not the same spiral as the one of the shell. This internal spiral affects the digestive system as well. With its mouth to the ground, the snail is infamous for the positioning of the anus above the mouth on the right side of the head (Figure 2).

In snails, the mantle secretes a shell, and this requires calcium carbonate. For this reason, you will find a number

of terrestrial taxa restricted to limestone areas. Slugs (Figure 3), on the other hand, lack shells and exhibit no external twists. Instead they have a thin calcareous plate embedded in the mantle.

Unlike the marine snails, terrestrial gastropods lack an operculum to cover the shell opening. Instead, they use a calcified slime (epiphragm; Figure 4) for protection in hibernation or aestivation. The respiratory pore (Figure 3) is on the right side of the body, and closes to keep out water in aquatic species or to prevent desiccation under dry conditions on land. Both aquatic and terrestrial gastropods have lungs, necessitating return to the surface for aquatic members to get air. Aquatic members have only one pair of non-retractile tentacles, whereas land-dwellers have two pairs and both are retractile. Aquatic species have an eye at the base of each tentacle; the land snails have their eyes on the tips of the rear pair of tentacles.

Most gastropods eat algae and plants, which they scrape with the radula (Figure 5), but a few are carnivorous. The radula is made of chitin with rows of minute calcareous teeth. And if you thought bryophytes used minute characters for identification, snail identification is often based on these teeth!

Chapter 4-8: Invertebrates: Molluscs 4-8-3

Figure 2. Snail, showing its major internal and external parts. Note the dart sac from which the love dart is ejected. Image from

Wikimedia Creative Commons.

Figure 3. Great Red Slug, Arion rufus, dark form, Bishop

Middleham Quarry Nature Reserve, Co Durham. Note the large respiratory pore on the mantle of this sometimes moss dweller. This snail can travel nearly 0.5 km in search of more suitable conditions (Sandelin 2012). Photo by Brian Eversham, with permission.

Figure 4. Helix pomatia epiphragm. Photo by Hannes

Grobe, through Wikimedia Commons.

Figure 5. Pomacea canaliculata mouth showing radula. Photo by S. Ghesquiere, through Wikimedia Commons.

Reproduction

Most terrestrial snails and slugs are simultaneous hermaphrodites, mutually exchanging gametes during copulation. This is not true for land-dwelling prosobranch snails (including the Pomatiidae, Aciculidae, Cyclophoridae, and others) – families that have separate sexes (Wikipedia 2012b). The prosobranch snails are the ones that have an operculum that can be used to cover the opening when they retreat into the shells.

Some land snails are sequential hermaphrodites, being first male, then female (Nordsieck 2012b). Others, such as Arianta arbustorum (Helicidae; Figure 6), a moss-dwelling snail, have a mechanism that prevents sperm cells from fertilizing the snail's own egg cells before they reach the sperm pouch of the mate. In the aquatic Lymneidae, snails can reproduce using unfertilized eggs, permitting


them to multiply rapidly in a new location and causing invasive species problems when they are introduced as aquarium pets.

The reproductive anatomy of the snail is a bit peculiar, with the penis and vagina everting from near the head (Figure 7-Figure 8). In the hermaphrodites, the penes wrap around each other, sometimes extending to great lengths (Figure 9).

Figure 6. Arianta arbustorum on a bed of mosses and leafy

liverworts. Photo ©Roy Anderson, with permission.

Figure 7. Helix pomatia head during mating. Redrawn from

Johannes Meisenheimer, through Wikimedia Commons.

Figure 8. Helix pomatia head after mating, showing both

male and female parts of this simultaneous hermaphrodite. Redrawn from Johannes Meisenheimer, through Wikimedia Commons.

Figure 9. Slugs mating, demonstrating the very long penes.

Photo through Wikimedia Commons.

Mating and the Love Dart

The mating process is a combination of love and war (Figure 10). The dart, or more than one in some species, is made of calcium carbonate, chiton, or cartilage (Figure 11). During mating, each snail tries to inject this "dart" into the other snail (Figure 12) (Koene & Chase 1998a; Chase & Blanchard 2006). It might be more appropriate to call this a dagger because it is injected by a thrust, not a shot or a throw. The first mating of a snail stimulates the production of the dart, so it cannot be used until the second mating. Once used, it requires time to generate a new one.

Figure 10. Roman snails (Helix pomatia) in full foot contact

during mating. This process of contact of foot, lips, and tentacles can take up to 20 hours. Photo through Wikimedia Commons.

Figure 11. Love dart of the snail Monachoides vicinus.

Photo by Joris M. Koene and Hinrich Schulenburg through Wikimedia Commons.


Figure 12. Mating garden snails (Helix aspera) with love

dart in snail on right, just above the antenna of the left snail. Photo by Eynar through Wikimedia Commons.

But what does the dart accomplish? Early hypotheses

considered it to be a "gift of calcium" to help in the development of the eggs. Leonard (1992) used a theoretical model to support the hypothesis that the love dart induced the partner to act as a male, hence insuring that the thruster would also be fertilized. Koene and Chase (1998a, b) used an experimental approach to disprove the long-held hypothesis of a "gift of calcium."

Through the work of Koene and Chase (1998 a, b), the role of this dart has become clearer. It carries with it a mix of hormones that help to move the sperm cells toward the sperm pouch where they are stored until fertilization (Koene & Chase 1998a, b). This is accomplished by causing changes in the structure of the copulatory canal leading ultimately to the sperm pouch. These changes increase the chances, often doubling them, that sperm from that mating snail are successful in fertilizing eggs, since it is likely that the partner will have multiple mating events. But the dart, preferably aimed at the foot, can miss its ideal target and land in a less desirable location, like the base of the antenna. When that happens, the snail is no longer able to retract or extend the antenna.

Each partner goes through gyrations apparently in an attempt to avoid being recipient of the love dart, or at least to avoid receiving it in an undesirable location. So far, Leonard's (1992) hypothesis of stimulating the partner to carry out its male role does not seem to have been tested experimentally, but with the mix of hormones it could still be a viable part of the story. It appears that this love dart, although not understood at the time, could have been the basis for the story regarding Cupid's arrow (Chase 2010).

Egg and Larval Development

Most gastropods lay eggs, with only a few species bearing live young. In aquatic snails, development of the larva occurs as a planktonic stage once it leaves the egg, but in terrestrial pulmonate snails, development is completed within the egg. Some snails (e.g. Clausiliidae) exhibit ovoviviparity, wherein the larvae emerge inside the mother's body and emerge from "her" body as juvenile snails (Nordsieck 2012b). This practice permits these snails to live in dry areas where external eggs could not survive the desiccation. Some species of the oviparous (egg-laying) species, such Arion flagellus (Figure 13), lay their eggs under or among bryophytes (Figure 14).

Figure 13. Arion flagellus on a sheet of mosses. Photo ©

Roy Anderson <habitas.org.uk>, with permission.

Figure 14. Arion flagellus eggs in Oaks Wood, Cambourne, Cambridgeshire, UK. Note the bit of moss beside the eggs and on the eggs – remnants of the cover that previously protected them. Photo by Brian Eversham, with permission.

Richter (1972) found that the banana slug (Ariolimax columbianus, Figure 15) laid 3-4 mm eggs under moss where soil conditions were neither excessively wet nor dry. Placing eggs under mosses and other loose substrata may be an energy-saving strategy for some species. Bauer (1994) considered the behavior of some snails that dig holes to be an investment in parental care, but incurring an energy cost. Other than these preparations, snails do not tend their eggs or hatchlings. Ariolimax californicus (Figure 16) also may occur under bryophytes (Peggy Edwards, pers. comm.).


Figure 15. Ariolimax columbianus on moss. Photo by Bill

Leonard, with permission.

Figure 16. Ariolimax californicus exiting a mat of mosses, a suitable location for laying eggs. Photo coourtesy of Peggy Edwards.

Bryophyte Interactions

Glistening trails of pearly mucous (Figure 17) criss-cross mats and turfs of green, signalling the passing of snails and slugs on the low-growing bryophytes (Figure 1). In California, the white desert snail Eremarionta immaculata (Figure 18) is more common on lichens and mosses than on other plant detritus and rocks (Wiesenborn 2003). Wiesenborn suggested that the snails might find more food and moisture there. Are these molluscs simply travelling from one place to another across the moist moss surface, or do they have a more dastardly purpose (as hunters) for traversing these miniature forests?

Figure 17. Lehmannia valentiana with its slime trail on a

moss (upper right) in Swavesey, Cambridgeshire, UK. Photo by Brian Eversham, with permission.

Figure 18. Eremarionta immaculata in the Riverside

Mountains, CA, USA. Photo by William D. Wiesenborn, with permission.

But not all snails and slugs find the bryophyte substrate attractive. Some actually avoid its rough surface. Nevertheless, trails of slime (Figure 19) are not unusual, and we have little insight into the reasons why some find it inviting while others find it repulsive.

Figure 19. Snail or slug trails on Dicranum viride on big

maple trunk. Photo courtesy of Betsy St. Pierre.

Abundance

Snails can sometimes occur in significant numbers in moss habitats. Their need for a moist environment (Pratt 1935) would seemingly attract snails to the mosses as a moist substrate. Quantitative information on snails and slugs among bryophytes is scarce, and often only mentions that bryophytes are abundant in the habitat (e.g. Nekola 2002).

The study by Grime and Blythe (1969) is helpful in understanding numbers and dynamics of moss-dwelling snail populations, but we need many more studies. They found average morning populations of up to 8.5 per 100 g dry weight of moss in early September for the copse snail Arianta arbustorum (Figure 20) at Winnats Pass in Derbyshire, England. In collections totalling 82.4 g of moss, they examined snail populations in a 0.75 m2 plot each morning on 7, 8, 9, & 12 September 1966. Arianta arbustorum numbered 0, 7, 2, and 6 on those days, respectively, with weights of 0.0, 8.5, 2.4, and 7.3 per 100 g dry mass of moss. This was surpassed only by those on


Urtica dioica (stinging nettle) reaching 14.4 and Mercurialis perennis (dogs mercury) reaching 16.2.

evertheless, it takes a lot of dry moss to make 100 g. N

Figure 20. The moss-dwelling copse snail, Arianta arbustorum. Photo © Roy Anderson <habitas.org.uk>, with permission.

Nighttime activity by many snails is likely to be greater than that during the day, and little snails may actually seek refuge in mosses during the day (Grime & Blythe 1969). Furthermore, snails like Arianta arbustorum (Figure 20) typically climb, often to a considerable height, to obtain food. Bryophytes just don't fit as a refuge for larger snails, so the behavior of the larger Arianta arbustorum may not reflect that of the small snails.

Adaptations

Confusing the Predator

In the Pacific Northwest, USA, unusual jumping slugs in the genus Hemphillia (Figure 21-Figure 24) prefer coarse woody debris or moss mats on decaying logs (Leonard & Ovaska 2003). They have some remarkable adaptations for their log habitats. One such adaptation appears to be to confuse their predators by smearing their lime trail (s Figure 17).

Figure 21. Hemphillia glandulosa, the warty jumping slug, on moss. This and the following photo illustrate the variability in its coloration. Photo by Kristiina Ovaska, with permission.

Jumping to Escape

A second adaptation to avoid predation is to "jump." Jumping slugs (Hemphillia; Figure 22) don't actually jump. Instead, when they are approached by a predator snail or other predator, they tighten their muscles, coil up, and straighten rapidly, flopping around on their substrate until they are free of it, and fall. This effects a rapid motion that looks like a jump (Leonard 2011). This activity also breaks the slime trail, facilitating their freedom to "jump." The slow-moving predator snails don't have a chance. Leonard says these slugs are potentially successful dispersers of fungal spores. I would think that would work for dispersing bryophytes as well, for spores, asexual structures, and fragments.

Figure 22. Hemphillia glandulosa, the warty jumping slug,

on moss. This and the above photo illustrate the variability in its coloration. Photos by Kristiina Ovaska, with permission.

In Canada, some of these Hemphillia (Figure 21-Figure 24) species seem safe from extinction due to sufficient abundance, but others are endangered due to increasing patchiness of suitable habitats (Leonard & Ovaska 2003). The 1994 NW Forest Plan regulates ground disturbance activities on federal lands in northern California to Washington, protecting "survey and manage" species, including several species of jumping slugs, Hemphillia. Hemphillia dromedarius (dromedary snail; Figure 23-Figure 24) is officially threatened in both Canada and the United States, where it lives in the state of Washington. Legal protection of these slugs can help in the protection of mosses in these areas. However, the Bush administration was not sympathetic to this protection and it could be lost at any time with a change in administrative philosophy. Perhaps the novelty of its jumping behavior will increase public interest and sympathy and lead to its protection in yet another way.

Figure 23. Hemphillia dromedarius, the dromedary jumping

slug. Photo by Kristiina Ovaska, with permission.


Figure 24. Eggs of Hemphillia dromedarius, the dromedary

jumping slug. Photo by Kristiina Ovaska, with permission.

Keeping It Small

If you want to go clambering among the bryophytes, it helps to be small (Figure 26). One would expect that size would also constrain movement among the bryophytes and restrict larger snails to the surface. But some tiny snails actually occur fairly deep within the bryophyte mat. Such is the elongate snail captured by Jan-Peter Frahm deep within a cushion of Distichium capillaceum (Figure 25).

Figure 25. Distichium capillaceum with a snail nestled deep

within the cushion. Photo by Jan-Peter Frahm, with permission.

Truncatellina cylindrica (Figure 26) is another very small snail. Where it lives at Groomsport, Down, UK, it occurs in yellow dunes among mosses and the roots of vegetation on drier, sunny slopes (Anderson 1996).

Figure 26. Truncatella cylindrica on Tortula sp. Note the

small size of this conical snail. Photo by Stefan Haller, with permission.

Szlavecz (1986) determined that snail size plays an important role in their behavior, including food searching. Although one might think that larger animals need to eat more, it seems that the larger Monadenia hillebrandi mariposa (Figure 27) instead spends more time crawling and less time feeding, permitting it to travel farther. Although it prefers leaf litter, it consumes mosses as well (Figure 28). This snail lives in cool, mossy forests and sometimes hibernates among mosses, including thick moss on a bigleaf maple branch (Sandelin 2012).

Figure 27. Monadenia hillebrandi, a consumer of the

mosses Rhytidiadelphus sp. and Grimmia trichophylla. Photo by John Slapcinsky, through Creative Commons.

Figure 28. Laboratory selection of foods by the snail Monadenia hillebrandi mariposa. Upper: all data combined. Lower: juveniles vs adults. Redrawn from Szlavecz 1986.


Monadenia fidelis (Figure 29) lives in dry forests as well as prairie wetlands where its presence is indicative of an unburned prairie (Severns 2005). Loubser et al. (2005) found it associated with nearby mosses in 33% of their samples. But like many observations of animals with bryophytes, this may mean that they need bryophytes in their habitat, that they prefer the same habitats as bryophytes, or that the relationship is coincidental – the bryophytes are near something they need. In this case, mosses are one of its winter hibernating sites, where they hibernate under mosses in crotches of maple trees (Monadenia 2016).

Figure 29. Monadenia fidelis (Pacific sideband snail) on

mosses. Photo by Walter Siegmund through Wikipedia Commons.

Conical Shape

The terrestrial conical snails, or at least the smaller of these snails, seem to be more suited to traversing the internal spaces of bryophytes. Cochlicopa lubrica (Figure 30) and Cochlicopa lubricella (Figure 31), moss snails, have been known from mosses for a long time. In 1840 Turton reported these snails from mosses and grass on the ground and under stones in the British Isles.

Figure 30. Cochlicopa lubrica on mosses. Photo by

Malcolm Storey, through Creative Commons.

Figure 31. Cochlicopa lubricella, moss snail, on mosses.

Photo © Roy Anderson <habitas.org.uk>, with permission.

Turton (1840) also reported another tiny conical snail, Ena obscura (Figure 32), from mosses and under stones. But this snail has another way to be elusive from would-be predators. It covers itself with mud or debris, rendering it nearly invisible by hiding the shiny shell (The Great Snail Hunt 2012), but might it also provide a means of controlling water loss or temperature?

Figure 32. Ena obscura, a snail that lives in forests or on

walls, under stones and moss (Turton 1840) in the Sulehay, Northants, UK. It covers itself with mud as camouflage. Photo by Roger S. Key, with permission.

Avoiding Desiccation

Bryophytes remain moist long after their epiphytic and rock substrata, and even those on dry soil can become moist, collecting fog or light rainfall that never reaches the soil. Hence, they can become a refuge for snails and slugs seeking moisture. Such is often the case for the banana slug, Ariolimax columbianus (Figure 15), in the Pacific lowlands, USA. This slug leaves its moist cover on a moss-covered fallen log to forage at night, then returns to the moss (Sandelin 2012). Taking advantage of the


moisture at night, this slug can travel nearly 0.5 km in search of more suitable conditions.

The large (up to 13-15 cm) bryophyte-dwelling slug Arion ater (Figure 33-Figure 35) forms a ball by contracting its body and humping up (Figure 34) (Sandelin 2012). That reduces its surface area and thus reduces water loss. It can also twist on itself to reduce exposed surface area (Figure 35). This twisting ability is probably also helpful as it climbs moss setae and feeds on the capsules.

Figure 33. Black form of Arion ater in an extended position.

Photo by David Perez, through GNU Free Documentation.

Figure 34. Black form of Arion ater forming a ball by contracting and humping up. Photo by Emőke Dénes, through Wikimedia Commons

Figure 35. Arion ater juvenile contracting on itself. Photo

© Roy Anderson <habitas.org.uk>, with permission

Bryophytes can offer the snails and slugs yet another means to escape drought and extreme heat or cold. These gastropods can hibernate in cold temperatures or aestivate in heat or drought (Boss 1974), and this sometimes occurs

among bryophytes. Some snails remain dormant for as many as five or six years. Boss suggests that the ability to hibernate and aestivate may play a strong role in the expansion of geographic range, speciation, and extinction.

The European snail species Fruticicola fruticum (=Eulota fruticum, Bradybaena fruticum; Figure 36) hibernates from October until a time in spring when the weather is suitable for it to become active (Künkel 1928). It accomplishes this hibernation in dead moss or it may burrow into the ground with its aperture facing upward.

Figure 36. Fruticicola fruticum with Polytrichum nearby.

Photo by Michael Becker, through Wikimedia Commons.

No Shell – Slugs

Slugs can be somewhat common on bryophytes and seem to have the same adaptations as snails. Their only advantage would seem to be greater flexibility due to the absence of a hardened and bulky shell, but that brings with it a greater chance for desiccation. For many species, being small helps in permitting them to hide from predators and to maneuver among the bryophytes (Figure 37).

Figure 37. Keeled slug (Tandonia budapestensis), common

inhabitant of mosses such as this Leucolepis in the Pacific Northwest, USA. Photo courtesy of Jeri Peck.

The Limacidae is a family of slugs, and both common genera (Deroceras, Limax) have members that have been found among mosses. In the sub-Antarctic Marion Island, the slug Deroceras panormitanum (Figure 38; originally described as the separate species D. caruanae) lives in moist bryophyte communities as well as on decaying bryophytes (Smith 1992). With a totally exposed body, slugs in such harsh environments can find shelter and moisture among the bryophytes.


Figure 38. Deroceras panormitanum on what appears to be

a species of the moss Campylopus. Photo © Roy Anderson <habitas.org.uk>, with permission.

Brain Eversham (pers. comm. 21 March 2012) tells me that the yellow slugs, Limax flavus (=Limacus flavus; Figure 39) and L. maculatus (Figure 40), live mainly on old walls in Britain, where, like many snails, they are night active. They feed primarily on lichens and algae, but will graze on dead plant material if they run out of lichens. They don't generally eat leafy mosses, but they will browse on the capsules. He has observed Tortula muralis (Figure 41) and Grimmia pulvinata (Figure 42) with the setae remaining but all the capsules nibbled off. He suggests that the capsules and spores are more nutritious or more

igestible than the leaves and stems. d

Figure 39. Limax flavus on a bed of mosses. Photo © Roy Anderson <habitas.org.uk>, with permission.

Figure 40. Limax maculatus on moss at Bridge House,

Swavesey, UK. Photo by Brian Eversham, with permission.

Figure 41. Tortula muralis, a species whose capsules serve

as food for species of Limax. Photo by Michael Lüth, with permission.

Figure 42. Grimmia pulvinata with capsules and awns.

Photo by Michael Lüth, with permission.

In Search of Food

As just described for two species of Limax, snails and slugs may browse on bryophytes. They have a rasping tongue (radula) that destroys the epidermis of tracheophytes (Grime & Blythe 1969), but what does it do to moss leaves only one cell thick? Apparently in some cases it makes mosses potential food (Szlavecz 1986), and enables some gastropods to consume even the tough capsule (Davidson & Longton 1987, Davidson et al. 1990).


Guy Brassard reported to me that Stéphane Leclerc has taken a picture of a slug in Quebec, Canada, eating a Buxbaumia aphylla (Figure 43-Figure 44) capsule! Michael Lüth (Bryonet 23 September 2017) observed and photographed a slug grazing on the capsule of Buxbaumia viridis (Figure 45). Dave Kofranek reports tasting it – it tastes like cucumbers (Bryonet 24 September 2017).

Figure 43. Buxbaumia aphylla that are immature and have

not been eaten. Photo by Štĕpán Koval, with permission.

Figure 44. Buxbaumia aphylla that may have been damaged

by a herbivore. Photo by Janice Glime.

Figure 45. Buxbaumia viridis with slug eating capsule.


Low Palatability?

Often it appears that the palatability index for bryophytes is low (Jennings & Barkham 1975). Furthermore, snails and slugs seem to be less interested in grazing things with awns than those without. Robin Stevenson (pers. comm. January 2008) has seen Bryum argenteum (Figure 46-Figure 47) that is completely grazed over, but never observed such grazing on an awned Grimmia species (Figure 42). Could it just be that there is no nutrition in an awn, or do they have trouble gliding across the furry tips of leaves?

Figure 46. Bryum argenteum, a moss with no awns and a

food source for snails and slugs. Photo by Michael Lüth, with permission.


Figure 47. Bryum argenteum showing lack of awns. Photo

from UBC website, with permission from Shona Ellis.

But awns, even in Grimmia pulvinata (Figure 48), may not deter all snails (Figure 48). Szlavecz (1986) was able to identify the awned Grimmia trichophylla (Figure 49) in the feces of the California snail, Monadenia hillebrandi mariposa (Figure 27) and also demonstrated that the spine tips of the tracheophyte Selaginella hansenii (Hansen's spikemoss; Figure 50) did not deter feeding or crawling. Perhaps it depends on the density of the hair tips, since Grimmia trichophylla (Figure 49) and S. hansenii (Figure 50) have much less dense hairs than G. pulvinata (Figure 48), and on the particular species and size of snail or slug. On the other hand, it appears that the slugs are able to graze the lower margins of a clump, apparently resting on the substrate without the need to traverse the awns (Figure 48).

Figure 48. Grimmia pulvinata exhibiting grazing that girdles the base of the clump in a pattern typical of snail or slug grazing, but also known for isopods. Photo by Robin Stevenson, with permission.

Michael Lüth has observed snails grazing on Orthotrichum (Figure 51) and Terry McIntosh has seen slugs grazing on other bryophytes, with both observers indicating that the damage to the moss was similar to that

shown for Grimmia pulvinata in Figure 48 (Bryonet 12 January 2008). On the other hand, Frank Greven (Bryonet 13 January 2008) has seen this pattern as a result of grazing by isopods (wood lice). Robin Stevenson (pers. comm. 14 January 2008) agrees that isopods might be deterred by the awns, causing them to eat in such a pattern. But in this case, after climbing up a bridge coping, the snail or whatever might have found that this moss provided the best choice available.

Figure 49. Grimmia trichophylla in Bretagne (Brittany),

France, showing somewhat less imposing awns than those of Grimmia pulvinata. Photo by Michael Lüth, with permission.

Figure 50. Selaginella hansenii, a spine-tipped tracheophyte

eaten by the snail Monadenia hillebrandi mariposa. Photo by J. E. (Jed) and Bonnie McClellan © California Academy of Sciences, with permission.

Figure 51. Orthotrichum urnigerum, member of a genus

known to be grazed by snails. Photo by Michael Lüth, with permission


Low Nutritional Quality?

That rasping tongue is not always enough to accomplish the task of obtaining nutrients from mosses. Oyesiku and Ogunkolade (2006) experimented with snails and the moss Bryoerythrophyllum campylocarpum. In laboratory experiments, snails (Limicolaria aurora; Figure 52) gained the most weight when fed Bryoerythrophyllum campylocarpum paste. Snails that had only unground moss actually lost weight. Those in the field experiment (restricted to B. campylocarpum) either lost weight or remained the same. Fecal matter of field snails had fragments of moss that had lost chlorophyll from their cells as well as that of abundant algae and Cyanobacteria. Presence of snails on the moss was seasonal from April until October, when moisture and lower temperature of the moss may have provided favorable habitat. This experiment suggests that in this case the snail was unable to penetrate the cells of the moss, making it an unlikely food source in nature. Rather, the researchers suggest that snails most likely use moss as a moist and cool habitat.

Figure 52. Shell of Limicolaria aurora. Photo by David G. Robinson, USDA APHIS PPQ at Bugwood.org, through public domain.

Food for Some

Clearly for some slugs and snails there are bryophytes that do indeed seem palatable. Ochi (1960) reported that the thallose liverwort Conocephalum conicum (Figure 53) served as food for a slug. Merrifield (2000) found evidence of heavy grazing on epiphytic bryophytes, particularly the moss Syntrichia laevipila (Figure 54), of Oregon white oaks (Quercus garryana) in the Willamette Valley, Oregon, USA, and considered that either springtails or slugs were likely responsible. She considered that the abundance of gemmae on S. laevipila may be a response to this grazing.

Figure 53. Conocephalum conicum showing feeding

damage upper middle) by something, perhaps a slug. Photo by John Hribljan, with permission.

Figure 54. Syntrichia laevipila on bark. Photo by Jonathan

Sleath, with permission.

Algae growing on mosses, especially in the aquatic habitat, could be a prominent source of food for gastropods. In the Negev Desert, adult desert snails (Sphincterochila zonata) fed exclusively on algae on the soil surface, creating an algal turnover of 142 kg hectare-1, despite being active for only 8-27 days in winter during the rainy period (Shachak & Steinberger 1980). Other Negev Desert snails feed on the mosses themselves. Sphincterochila boissieri (Figure 55) feeds on shrubs there, but its feces indicate that it also feeds on the moss Tortula atrovirens (=Desmatodon convolutus; Figure 56) (Yom-Tov & Galun 1971). This is a snail that has color morphs of brown and white, but they apparently don't affect its temperature (Yom-Tov 1971; Slottow et al. 1993). However, their rodent predators choose more brown than white snails, enough to be significantly different (Slottow et al. 1993).

Figure 55. Sphincterochila boissieri, a species that is known

to eat Tortula atrovirens in the Negev desert. Photo by Mark A. Wilson, through Creative Commons.

Figure 56. Tortula atrovirens, a moss that is eaten by the

Negev Desert snail, Trochoidea seetzeni. Photo by Des Callaghan, with permission.


Szlavecz (1986) examined feeding preferences in 31 individuals of the snail Monadenia hillebrandi mariposa (Figure 27). Collections of field feces indicated that they consumed the mosses Rhytidiadelphus sp. (Figure 57) and Grimmia trichophylla (Figure 58) in nature, among other things. In the lab, they preferred shrub and bay litter over mosses, but preferred mosses and lichens over grasses and pine litter. More green moss than brown occurred in the feces, whereas brown material was more common from consumed tracheophytes (Figure 59).

Figure 57. Rhytidiadelphus squarrosus, a member of a

genus that has been found in feces of the snail Monadenia hillebrandi mariposa. Photo by Michael Lüth, with permission.

Figure 58. Grimmia trichophylla showing awns. Photo by

Michael Lüth, with permission.

Grime and Blythe (1969) found bryophytes in the feces of four species of snails out of the six examined from Winnats Pass, Derbyshire, England, on 13 October. But then, tracheophyte foods often become less nutritious as the plants prepare for winter. Studies by Chatfield (1973), Williamson & Cameron (1976), and Richter (1976) indicate that at least juvenile snails might do best on a mixed diet. But for Cepaea nemoralis (Figure 60-Figure 61), it appears that even though mosses are part of their habitat, they are seldom part of the diet (Williamson & Cameron 1976).

Figure 59. Comparison of green and brown portions of plant

material eaten by the snail Monadenia hillebrandi mariposa. Modified from Szlavecz 1986.

Figure 60. Cepaea nemoralis, banded snail juvenile at Old

Sulehay Forest, UK, a species that lives in a mossy habitat but apparently does not eat them. Photo by Brian Eversham, with permission.

In the tropical montane rainforest of Brazil, those small, flattened snails in the Charopidae (Figure 62) eat bryophytes (Maciel-Silva & dos Santos 2011). Both Canalohypopterygium tamariscinum (syn. = Hypopterygium tamarisci; Figure 63) and Lopidium concinnum (Figure 64) had evidence of leaf herbivory,


mostly in the beginning of the rainy season (September to December). A species of snail in the Charopidae and a moth larva in the Geometridae were the culprits. Using an index of damage (ID) in 2007, 2008, Maciel-Silva and dos Santos found that C. tamariscinum had higher damage (68%, 35%) than L. concinnum (38%, 23%) in these two years (Figure 65). These rates were lower than those for tracheophytes. They found no correlation with phenols, proteins, or the ratio between them (Figure 65).

Figure 61. Cepaea nemoralis, a species that lives in a mossy habitat but apparently does not eat them. Photo by Stefan Haller, with permission.

Figure 62. Charopidae feeding on Lopidium concinnum from an Atlantic Forest, Brazil. Photo by Adaises Maciel-Silva and Nivea Dias dos Santos, with permission.

Figure 63. Canalohypopterygium tamariscinum, a food

source for Charopidae. Photo by Niels Klazenga, with permission.

Figure 64. Evidence of Charopidae herbivory on Lopidium

concinnum from an Atlantic Forest, Brazil. Photo by Adaises Maciel-Silva and Nivea Dias dos Santos, with permission.

Figure 65. Charopidae and Geometridae damage to

mosses in 10 colonies of plants. Image from Adaises Maciel-Silva and Nivea Dias dos Santos.


An Avoidance of Gametophores?

Davidson and Longton (1985, 1987; Davidson 1988, 1989) reported that several species of generalist slugs consumed bryophytes. In some cases, the protonema (threadlike stage that develops from moss spore) is readily consumed (Grime 1979). In Great Britain, capsules and protonemata of several mosses [Brachythecium rutabulum (Figure 66), Mnium hornum (Figure 67-Figure 68), and Funaria hygrometrica (Figure 69)] were eaten preferentially to leafy gametophores by slug species in the genus Arion (Figure 70) (Davidson & Longton 1987; Davidson et al. 1990). Cambs (2012) found that the slug Limax maculatus (Figure 40) likewise would eat capsules, but the leafy parts seemed to serve only as an emergency food. It appears that some may even eat calyptrae (covering over capsule; Figure 71). Ferulic acid, present in shoots but absent in young capsules of Mnium hornum, is a phenolic compound that is only released after severe hydrolysis. Its antibiotic role as an antifungal agent (Sarma & Singh 2003) and in antiherbivory (Seigler 1983; Smith 2011) may contribute to this preference for capsules, as discussed below. Davidson and coworkers found that older capsules with spores were less preferred than the green ones (Figure 72; Davidson & Longton 1987; Davidson et al. 1990).

Figure 66. Slug eating capsules of Brachythecium. Note the number of setae that are missing capsules. Photo by Janice Glime.

Figure 67. Young, green capsules of Mnium hornum that

are preferred by Arion slugs. Photo by Michael Lüth, with permission.

Figure 68. Mature capsules of Mnium hornum. Photo by

Janice Glime.

Figure 69. Capsules of Funaria hygrometrica – potential snail food. Photo by Michael Lüth, with permission.

Figure 70. Arion rufus on mosses in a woodland above

Poole's Cavern, Buxton, UK. Photo by Brian Eversham, with permission.

Figure 71. Slug on moss calyptra, apparently finding

something to eat. Photo courtesy of Sarah Lloyd.


Figure 72. Relative damage by slugs (Arion spp.) of sporophyte stages of two species of bryophytes. n=300-500 at day 0. LCI = late calyptra stage; EOI = early operculum intact; LOI = late operculum intact; OF = operculum fallen; EF = empty and fresh. Redrawn from Davidson et al. 1990.

The slugs consumed only trivial amounts of Brachythecium rutabulum shoots (Figure 66; Davidson 1989). Mnium hornum (Figure 77) was also ignored, but after 5-7 days of starvation Arion rufus (10-15cm long; Figure 73) and A. subfuscus (5-7 cm long; Figure 75) ate significant quantities of shoots of this species. The garden slug Arion hortensis (Figure 74) still ignored the moss even after 7 days of starvation.

Figure 73. Arion rufus on a bed of mosses. Photo by Jean

Bisetti, with permission.

Figure 74. Arion hortensis s.s. at Bridge House, Swavesey,

UK. Photo by Brian Eversham, with permission.

Figure 75. Arion subfuscus, a slug known to consume

Mnium hornum. Photo by Gary Bernon, USDA APHIS at Bugwood.org, through public domain.

Presence of moss cells of Brachythecium rutabulum (Figure 76) and Mnium hornum (Figure 77-Figure 78) in the feces of previously starved Arion suggest that the leafy mosses are not digested well (Davidson et al. 1990). On the other hand, all three species of slugs named above readily consumed Funaria hygrometrica (0.4-6.5 mg wet weight per slug; Figure 69) in overnight feeding trials. The importance of mosses as food may rest with the organisms living on the mosses – fungi, bacteria, protozoa, rotifers, etc., making indigestibility of the mosses inconsequential.

Figure 76. Brachythecium rutabulum cells as they might be

seen in feces. Photo by Tom Thekathyil, with permission.

Figure 77. Mnium hornum shoots – a species that was

ignored in experiments until the slugs were starved. Photo by Janice Glime.


Figure 78. Mnium hornum leaf tip cells, what one might see

in feces. Photo by Bob Klips, with permission.

It is perhaps not surprising that snails eat the capsules of Splachnum (Figure 79). This genus has odors that attract flies, so they may serve as attractants to gastropods as well.

Figure 79. Snail on setae of Splachnum capsules in Alaska, eating capsules. Photo courtesy of Blanka Shaw.

Indirect evidence suggests that slugs and snails graze capsules of Buxbaumia viridis (Gordon Rothero, Birds feeding on moss capsules, Bryonet-l, 10 April 2003; Figure 80). Stark (1860) relayed a story of the ill fate of collected specimens of Buxbaumia aphylla (bug-on-a-stick moss; Figure 81) on their journey from Scotland to England. A slug had inadvertently been included in the package and it managed to destroy their prized specimens. On the other hand, B. aphylla can fool you. After repeated observations with my graduate student, Chang-Liang Liao, we have discovered in the field that what appeared to me to be grazing on capsules of Buxbaumia aphylla is really only the splitting of the capsule top as it dries (Figure 81), and that this occurs on nearly every capsule.

Figure 80. Buxbaumia viridis capsules. Note that the leafy

part belongs to another species of moss. Photo by Adolf Ceska, with permission.

Figure 81. Buxbaumia aphylla showing exposed green

spores in the capsule that has split open. Photo by Janice Glime.

Slugs also eat hornworts (Anthocerotophyta; Figure 82). Bisang (1996) reported that they especially eat the green sporophytes.

Figure 82. Phaeoceros carolinianus, a hornwort with mostly green sporophytes, a food source for slugs. Photo by Michael Lüth, with permission.


Deterrents to Herbivory

Longton (pers. comm. 1996) has speculated that phenolic compounds that protect the leafy gametophytes deter herbivory, especially on perennials. This could account for greater herbivory on the annual Funaria hygrometrica (Figure 83) than on perennial Brachythecium rutabulum (Figure 66) or Mnium hornum (Figure 77). The phenolic compounds in the latter two species were released only after severe hydrolysis, leading Davidson et al. (1990) to suspect that the phenolic acids might be tightly bound to cellulose in the cell wall. The greater palatability of the F. hygrometrica supports the general theory that perennials invest more resources in defense against herbivory than do annuals such as F. hygrometrica.

Figure 83. Young sporophytes of Funaria hygrometrica

before spores form. Photo by Michael Lüth, with permission.

Given the choice of capsules or vegetative material, both Arion rufus (Figure 3, Figure 70, Figure 73) and A. subfuscus (Figure 84) preferred immature capsules (see Figure 85 with a slug on immature capsules of Leucolepis acanthoneuron) of all three mosses, with Mnium hornum (Figure 77) being top choice (Davidson 1989). Setae were generally ignored, but A. subfuscus did occasionally eat M. hornum and Brachythecium rutabulum (Figure 66) setae. All three slugs also ate protonemata in the laboratory, and for B. rutabulum and Funaria hygrometrica (Figure 83) the protonemata were eaten just as much by A. rufus and A. subfuscus as were immature capsules. In fact, dry weight consumption exceeded that of immature capsules. Young shoots were also eaten, but less readily.

Figure 84. Arion subfuscus, a slug that prefers immature

capsules. Photo by Sanja 565658, through Creative Commons.

Figure 85. Slug browsing on immature capsule of the moss Leucolepis acanthoneuron. Photo from UBC website, with permission.

Davidson and Longton (1987) suggested that Arion hortensis (Figure 74) was restricted by the physical structure of the capsule to consuming developing spores from broken capsules in Polytrichum commune (Figure 86); no spores were eaten from unbroken capsules. When approaching Mnium hornum (Figure 77), the slugs would withdraw their tentacles, then retreat, suggesting some sort of chemical deterrent; they behaved similarly in the presence of extracts from the capsule. It is likely that hydroxycinnamic and phenolic acids in this species and in Brachythecium rutabulum (Figure 66) provided this chemical protection against herbivory (Davidson et al. 1989). Stems of both species were apparently protected by ferulic and possibly m- and p-coumaric acids bound in the cell walls of the shoots (Davidson et al. 1989), explaining the preference of the slugs for capsules. On the other hand, when moss extracts were placed on communion wafers, the slugs ate them more readily, suggesting that chemistry alone was not the likely deterrent (Anonymous 1987; Davidson et al. 1990). Rather, some physical feature of the mosses, perhaps the cell wall, deterred these slugs.


Figure 86. Polytrichum commune capsules showing the

persistent hairy calyptra and waxy capsule that is only eaten by snails when the capsule is broken. Photo by Michael Lüth, with permission.

Digestibility

So what did the slugs derive from the consumed mosses? When they consume preferred foods such as lettuce leaf or carrot root, the resulting feces contain macerated, partially pigmented tissue (Davidson 1989). When they consumed bryophytes, on the other hand, large pieces of leaf, whole leaves, and even stem pieces remained intact. Most cells still contained green chloroplasts. Evidently the moss did little more than fill the gut. Even the preferred capsules were poorly digested, with capsule wall fragments, opercula, and peristome teeth remaining. Mature spores seemed unharmed, but immature spores seemed to have experienced some digestion, appearing broken, colorless, and shrivelled. Likewise, the protonemata seemed to be digestible, resembling the lettuce and carrots in being macerated and colorless or brown.

Caution must be used in conducting laboratory experiments with food choices. Jennings and Barkham (1975) found that bryophytes all gave low palatability scores when six species of slugs, including the three in the Davidson (1989) study, had a choice of foods. The wider range of choices in the field may permit them to avoid the less palatable bryophytes.

Role in Bryophyte Competition with Lichens

Rosso and McCune (2003) found that molluscs on shrubs in the Pacific Northwest, USA, exhibited significant herbivore activity on the lichens. Bryophytes, on the other hand, had little change in cover between stems in exclusions and those available for herbivory. It appears that the mollusc herbivory on lichens (Boch et al. 2011) may benefit the bryophytes by contributing to the successful competition of the bryophytes over the lichens n the understory of these forests. i

Palatable Gametophytes

Des Callaghan (Bryonet 10 June 2011) reports slugs feasting on the gametophytes of Hookeria lucens (Figure 87) near a stream. In only six days they completely

removed all the plants by dining on them, leaving behind only a stump and a slime trail (Figure 88). This was a research station, so Callaghan needed to find a way to discourage the slugs. Suggestions from Bryonetters included sprinkling ground glass around the study area (Michael Richardson, Bryonet 10 June 2011); putting out cups of beer to attract and drown the slugs or putting curry powder or other hot substance around the mosses (Janice Glime, Bryonet 10 June 2011); copper rings that are effective in gardens and could be made with a coil of wire (David Bell, Bryonet 10 June 2011).

Figure 87. Hookeria lucens in healthy condition. Photo by

Des Callaghan, with permission.

Figure 88. Temperature/humidity data logger with Hookeria

lucens eaten by slugs. Photo by Des Callaghan, with permission.

Annie Martin (Bryonet 11 June 2011) is a professional gardener and described her experience in trying to eliminate slugs. She suggested putting salt on the head (if put on the tail the slug continues to live and eat). Her experience with beer is that it just keeps on attracting snails night after night, even though many of them drown, so it is an ineffective waste of money. Brown mulch seems to provide a favorable habitat, so she eliminated it, a technique that worked, but isn't relevant for discouraging nails on mossy rocks. s

Aquatic Grazing

Grazing by gastropods (slugs and snails) can be so severe as to define distribution of a bryophyte species. Lohammar (1954) found that in northern Europe Fissidens fontanus (Figure 89) was absent in lakes where Fontinalis antipyretica (Figure 90) was also absent. Gerson (1982) suggested that scarcity of Fissidens in some places is due to snail grazing. In the presence of Fontinalis, this smaller moss lives among the Fontinalis fronds where it is


presumably protected from snail grazing by the inedible forest of Fontinalis surrounding it and the density of the Fontinalis stems.

Figure 89. Fissidens fontanus, a moss that seems to be vulnerable to snail grazing except where it is protected by Fontinalis species. Photo by Michael Lüth, modified by Janice Glime, with permission.

Figure 90. Fontinalis antipyretica, a moss that apparently

protects the smaller Fissidens from grazing by snails. Photo by Bernd Haynold, through Wikimedia Commons.

It may be that in the aquatic habitat the snail effect on some bryophytes is much greater than in the terrestrial habitat. But it is not necessarily all bad. Steinman (1994) opined that snail grazing could account for the apparent unresponsiveness of epiphytes following phosphorus enrichment in a woodland stream in Tennessee, USA, where bryophytes were prominent. And some bryophytes seem prepared to fight back. The thallose liverwort Ricciocarpos natans (Figure 91) exhibits molluscicidal properties that are active against the snail carrier of schistosomiasis (Wurzel et al. 1990).

Figure 91. Ricciocarpos natans, a species with molluscicidal properties, floating on the water surface. Photo by Janice Glime.

Bryophyte Antifeedants

Based on the foregoing discussion, it appears that at least some bryophytes are able to discourage browsing by slugs (Frahm & Kirchhoff 2002). Alcohol extracts of the moss Neckera crispa (Figure 92) and leafy liverwort Porella obtusata (Figure 93) have antifeedant activity against the slug Arion lusitanicus (Figure 94). Extracts of 0.5% dry weight of the moss had low activity, whereas those from the liverwort exhibited moderate activity at only 0.05%. At 0.25% the antifeedant activity of Porella obtusata was complete. It is likely that this activity is not specific for slugs and may discourage insects, bacteria, and fungi as well.

Figure 92. Neckera crispa, a moss that has antifeedant activity against the slug Arion lusitanicus. Photo by Michael Lüth, with permission.

On the other hand, Arion lusitanicus (Figure 94), also known as the murder slug, easily eats the thallose liverwort Marchantia polymorpha (Figure 95) (Nils Cronberg, Bryonet 7 April 2016). Cronberg has observed this species feeding on Marchantia and has noticed that as the slug had invaded the wetland, Marchantia polymorpha had disappeared in parallel with the invasion.


Figure 93. Porella obtusata. Photo by Jan-Peter Frahm,

with permission.

Figure 94. Arion lusitanicus, a slug that traverses mosses, but finds Neckera crispa and Porella obtusata unpalatable. Photo by Mogens Engelund, through Wikipedia Commons.

Figure 95. Marchantia polymorpha showing a nibbled

thallus on the upper left, about 1/3 down and 1/3 over from the corner. It also has a tear that is not likely the result of herbivory. Photo by James K. Lindsey, with permission.

Dispersal Agents It appears that slugs are not all bad in the bryophyte

world and may instead be a necessary vector for some propaguliferous taxa (Stolzenburg 1995). Slugs and snails (Figure 96) leave a trail of mucous as they go, and as you well know if you have handled these molluscs, this

secretion can be sticky. It is therefore no surprise that these animals have dispersal abilities.

Figure 96. Snails such as this one traversing epiphytic

mosses in Japan may be effective dispersal agents. Photo by Janice Glime.

Slugs are able to disperse the brood branches of Dicranum flagellare (Figure 97) (Kimmerer & Young 1995). These tiny branches become entrapped in the secretions and are deposited in the ensuing slime trail. Kimmerer and Young found that these can be transported at least 23 cm from the colony, although the mean distance in their study was only 3.7 cm.

Figure 97. Dicranum flagellare showing the tight flagellate branches that can be dispersed by slugs. Photo by Janice Glime.

And it appears that the secretion increases the ability of the propagule to adhere to its substrate without affecting the germination rate. In fact, experiments by Davidson (1989) suggest that passage of spores through the slug's digestive system may enhance germination success. All plates containing mature spores from slug (Arion spp.; Figure 94) fecal pellets produced shoots, whereas only 80% of the plates with uneaten mature Mnium hornum (Figure 67-Figure 68) spores and 70% of those with uneaten Brachythecium rutabulum (Figure 98) spores produced shoots.


Figure 98. Brachythecium rutabulum, for which the spores

germinate better if they have passed through the gut of a slug (Arion). Photo by Michael Lüth, with permission.

For those snails and slugs that nibble on spores, one might assume that not all spores end up inside them. Unless they have perfect aim with that huge foot, their somewhat clumsy feeding method is undoubtedly going to render some spores as passengers in the mucous on the foot. Sooner or later, these will be deposited in a new location.

The ability of snails and slugs to glide across bryophytes and to climb setae to capsules suggests that these animals may be important as dispersal agents. But how widespread are herbivory and dispersal among bryophytes that temporarily host these slow-moving animals?

Although we know that bryophyte spores reach the mollusc gut, experiments are needed to see if spores expelled in feces are able to colonize successfully. Davidson (1989) found that Brachythecium rutabulum (Figure 98) and Mnium hornum (Figure 77) spores eaten by Arion species actually germinated better than controls.

Manfred Türke sent me images of mosses in the feces of the slug Arion vulgaris (Figure 99). I was amazed at the size of the fragment of moss in the feces (Figure 100-Figure 101). This is a potential means for dispersal, but the various species of bryophytes must be tested for viability. Digestive enzymes and extreme pH could damage the moss cells. On the other hand, the pathogenic fungi Phytophora spp. (Figure 102) survive as both oospores and filaments and are viable after passing through the digestive system of this slug species (Telfer et al. 2015). This was demonstrated by culturing the feces on agar.

Figure 99. Arion vulgaris, a slug that eats mosses,

potentially dispersing them. Photo by Dilian Georgiev through Creative Commons.

Figure 100. Arion vulgaris feces with bryophytes and other

material in it. Photo courtesy of Manfred Türke.

Figure 101. Arion vulgaris bryophyte from slug feces.

Photo courtesy of Manfred Türke.

Figure 102. Phytophthora parasitica zoosporangia, a genus

that survives passage through the gut of Arion vulgaris. Photo by Tashkoskip, through Creative Commons.

To provide additional information on the potential dispersal ability of slug feces, Boch et al. (2013) fed capsules of four bryophyte species [Bryum pallescens (Figure 103), Funaria hygrometrica (Figure 69), Leptobryum pyriforme (Figure 104), Pellia endiviifolia (Figure 105)] to three slug species [Arion vulgaris (Figure 99), A. rufus; Figure 3, Figure 70, Figure 73), Limax cinereoniger (Figure 106)]. Among the 117 bryophyte samples, 51.3 % of the spore cultures had germination following gut passage.


Figure 103. Bryum pallescens with capsules. Spores of this

species pass through the guts of several slugs and retain their viability. Photo by David T. Holyoak, with permission.

Figure 104. Leptobryum pyriforme with capsules. Spores

are able to pass through the guts of at least some slugs and remain viable. Photo by Michael Lüth, with permission.

Figure 105. Pellia endiviifolia with sporophytes. The spores

of this species are able to pass through the gut of several slug species and remain viable. Photo by Janice Glime.

Figure 106. Limax cinereoniger on a mat of moss. Photo

by Michal Maňas through Creative Commons.

Boch et al. (2013) found that germination rates did not differ among the bryophyte species, but the species of slug had strong effects. Among these three slugs, Limax cinereoniger (Figure 106) ate the lowest percentage of the bryophytes provided, and even correcting for that, they had the lowest percentage of feces samples (12.9%) producing protonemata. On the other hand, 76% of those of Arion vulgaris (Figure 99) and 74% of those of Arion rufus (Figure 3, Figure 70, Figure 73) produced protonemata (Figure 107).

Figure 107. Comparison of spore germination from

bryophytes cultured from the feces of three species of slugs. White bars = Arion rufus; light grey bar = Arion vulgaris, dark grey bar = Limax cinereoniger. Redrawn from Boch et al. (2013).

Türke et al. (2013) provide evidence that slugs do indeed disperse fragments of mosses by consuming spores and fragments. For tracheophyte seeds, they suggested an average of 5 m dispersal distance, exceeding the typical less than 1 m in dispersal by ants. In some slugs, the seeds are destroyed in the digestive tract, but in other cases they remain viable propagules.

Boch et al. (2015) discussed several ways that slugs benefit bryophytes. Their herbivory on tracheophytes (lignified vascular plants) permits more light to reach the low-growing bryophytes. But they also crawl across bryophytes and some eat the bryophytes. This puts them in the position to disperse spores, fragments, and other propagules.


Nevertheless, documentation of the effect of the slugs on the bryophyte community is meager. Boch and coworkers (2015) designed a factorial common garden experiment to determine some of the effects of slugs on the bryophyte vegetation. They collected sporophytes of 11 native and 1 invasive bryophyte species [Barbula convoluta (Figure 108), Brachythecium rutabulum (Figure 98), Brachythecium velutinum (Figure 109), Bryum sp. (Figure 103), Campylopus introflexus (Figure 110), Ceratodon purpureus (Figure 111), Funaria hygrometrica (Figure 69), Leptobryum pyriforme (Figure 112), Marchantia polymorpha (Figure 95), Phascum cuspidatum (Figure 113), Plagiomnium affine agg. (Figure 114), Pohlia sp. (Figure 115)], representing 8 families. They used three enclosure treatments: slugs previously fed with bryophyte sporophytes, slugs that had not been fed sporophytes, no slugs. The researchers demonstrated that bryophyte cover increased in 21 days from 1.4% to 3.9% in plots where slugs had been fed, an increase that was 2.8 times higher than in the other two treatments. After eight months, the species richness was 2.6X higher (5.8 vs 2.2) than in the other treatments. The researchers concluded that the slugs contributed to increasing bryophyte cover and diversity by reducing the dominance of tracheophytes. The early increase in cover in the enclosures with slugs fed sporophytes suggests that they also accomplish dispersal.

Figure 108. Barbula convoluta with capsules. Photo by

Kristian Peters, with permission.

Figure 109. Brachythecium velutinum with unopened

capsules. Photo by Michael Lüth, with permission.

Figure 110. Campylopus introflexus with capsules. Photo

by Michael Lüth, with permission.

Figure 111. Ceratodon purpureus with young capsules,

showing the normal proliferation. Photo by Michael Lüth, with permission.

Figure 112. Leptobryum pyriforme with numerous

immature capsules. Photo by Michael Lüth, with permission.


Figure 113. Phascum cuspidatum with unopened capsules.


Figure 114. Plagiomnium affine with developing capsules.

Photo by Jan-Peter Frahm, with permission.

Figure 115. Pohlia nutans with immature capsules. Photo

by Michael Lüth, with permission.

When the question of bryophyte dispersal by slugs arose on Bryonet, Scott Redhead (Bryonet 26 August 2016) suggested that this might even occur in the Splachnaceae. To that suggestion, Michael Lüth posted an image of Tetraplodon mnioides (Figure 116) showing one uneaten capsule and one that had been removed by an animal, possibly a slug, documenting his own observations of capsule herbivory. Christian Schröck (Bryonet 26 August 2016) likewise observed grazed capsules in Voitia and

Tetraplodon. However, we need observations of feeding to determine the identity of the herbivores.

Figure 116. Tetraplodon mnioides with one capsule eaten

by an unidentified herbivore. Photo by Michael Lüth, with permission.

Lüth (2010) suggested that the pre-dispersal stage of the capsules on Splachnaceae are likely to attract herbivores that differ from the flies that spread the spores. At this earlier stage, the capsules have a different odor from that during the dispersal stage. This odor lasts for only a short time and is therefore often missed by field biologists. On Bryonet (26 August 2016), Lüth explained that Splachnum ampullaceum smells like Vaccinium oxycoccos and occurs in the same habitats, often blending with these cranberries. And Tetraplodon mnioides (Figure 116) smells like Vaccinium myrtillus. Although not all evolutionary successes are linked to adaptation, it makes one wonder if these early odors are adaptive to facilitate a longer dispersal and subsequent deposition in dung, although one might assume that would require a larger mammal, not a slug.

Figure 117. Splachnum ampullaceum sporophytes with a

cranberry of similar color to the right. Photo by Michael Lüth, with permission.

I think most people would consider dispersal by snails and slugs to be distance-limited. But perhaps, with the help of birds, this is not so limited. Kawakami et al. (2003)


demonstrated that the Japanese White-eyes (Zosterops japonicus; Figure 118) and the Brown-eared Bulbuls (Hypsipetes amaurotis; Figure 119) are birds that eat snails. In fact, five species of snails are able to remain in their shells and appear in the feces. If these snails had eaten moss spores, those spores might be transported a considerable distance, yet be viable in the gut of the snail. It is probably a rare event. Lots of questions remain in this relationship, but the scenario brings up interesting hypotheses.

Figure 118. Zosterops japonicus, a bird that passes intact

snails through the gut. Photo by Dick Daniels, through Creative Commons.

Figure 119. Hypsipetes amaurotis, a bird that passes intact

snails through the gut. Photo by Nubobo, through Creative Commons.

Malone (1965) discovered another possibility, exemplified by the Killdeer (Charadrius vociferus; Figure 120). Malone found two species of freshwater snails attached to the feet of the Killdeer. These were able to remain attached and viable long enough to effect dispersal. The snail Galba obrussa was able to survive 14 hours on

Killdeer feet out of water. But the likelihood that an aquatic snail is carrying bryophyte spores is small due the rarity of capsules. Nevertheless, if a wetland snail has similar behavior, it has a better chance of having consumed spores from wetland mosses.

Figure 120. Charadrius vociferus, a species that disperses

snails on its feet. Photo by Andrew C, through Creative Commons.

One additional factor determining the suitability of a slug for spore (or fragment) dispersal is the habitat where feces are likely to be deposited. Researchers have made the first steps in understanding the role of slugs in bryophyte dispersal, but much remains to be explored.

Bryophytes as Home

Because of their small movement space, bryophytes can serve as safe sites for smaller snails. Birds can be significant consumers of snails, particularly during migration (Shachak & Steinberger 1980), and bryophytes can make the snails less conspicuous, if not hiding them completely. In terrestrial habitats, arachnids such as spiders and daddy-long-legs (Opiliones) are also predators on snails (Nyffeler & Symondson 2001). While some spiders can probably navigate the spaces within the moss mat, it seems unlikely that most mature daddy-long-legs could manage without getting caught. In addition to the arachnids, carabid beetles prey on terrestrial gastropods (Symondson 2004). Some of these beetles use a pump mechanism to extract the gastropod remains from its shell.

Even snails are predators on slugs. The shell of the snail makes navigation among the bryophyte branches more difficult, potentially making the bryophytes a refuge for the smaller of vulnerable slugs.

In a study of bryophyte inhabitants in the Bükk Mountains of Hungary, Varga (2008) found the tiny gastropods Punctum pygmaeum (Figure 121) and Pupilla muscorum (Figure 150) among the terrestrial mosses Plagiobryum zieri (Figure 122), Hypnum cupressiforme (Figure 123), and Tortella tortuosa (Figure 124). Standen (1898) found Punctum pygmaeum from moss shakings. From my own observations, it appears that snails and slugs are common on and even in bryophyte clumps, but finding


documentation on the use of bryophytes by these small species evades even the aggressive Google search.

Figure 121. The tiny Punctum pygmaeum on Ena

montanum, both on a moss. Photo by Stefan Haller, with permission.

Figure 122. Plagiobryum zieri, a moss that supports the

gastropods Punctum pygmaeum and Pupilla muscorum. Photo by Michael Lüth, with permission.

Figure 123. Slug on Hypnum. Photo by Janice Glime.

Figure 124. Tortella tortuosa in Europe. Photo by Michael Lüth, with permission.

The European snails Azeca goodalli (Figure 125), Euconulus fulvus (Figure 126), Columella edentula (Figure 127), Discus (subgen Goniodiscus) rotundatus (Figure 128), Lauria cylindracea (Figure 129-Figure 130, Vertigo pusilla (Figure 131), and Vitrina pellucida (Figure 132) live among mosses, among other substrata (Cloudsley-Thompson & Sankey 1961). Carychium tridentatum (Figure 133), Discus rotundatus, Cepaea hortensis (Figure 134), Oxychilus navarricus (formerly O. helveticus; Figure 135), and several rare species of Aegopinella (formerly in Retinella) [A. pura (Figure 136), A. nitidula (Figure 137-Figure 138)] are known under mossy brick rubble (Verdcourt 1954). Clausilia bidentata (10-11 mm; Figure 139) is also rare, but can be found under moss. Standen (1898) reported on Clausilia rugosa (Figure 140) swarming on mossy walls in the UK and feeding on mosses and lichens. Standen (1898) found the snail Acme lineata on a patch of the thallose liverwort Marchantia sp. (Figure 95).

Figure 125. Azeca goodalli shell. Photo by Francisco

Welter Schultes, through Creative Commons.

Figure 126. Euconulus fulvus. Photo by Brian Eversham,

with permission.


Figure 127. Columella edentula. Photo © Roy Anderson

<habitas.org.uk>, with permission.

Figure 128. Discus rotundatus on moss. Photo by

Christophe Quintin, through Creative Commons.

Figure 129. Lauria cylindracea on bark. Photo by


Figure 130. Lauria cylindracea, whose small size can be

seen in comparison to this seed. Photo by Christophe Quintin, through Creative Commons.

Figure 131. Vertigo pusilla on bark. Photo © Roy Anderson


Figure 132. Vetrina pellucida on bark. Photo © Roy Anderson <habitas.org.uk>, with permission.

Figure 133. Carychium tridentatum on moss-covered

branch. Photo © Roy Anderson <habitas.org.uk>, with permission.

Figure 134. Cepaea hortensis venturing into one of the

Pottiaceae mosses. Photo by Stefan Haller, with permission.


Figure 135. Oxychilus navarricus on the moss

Rhytidiadelphus squarrosus. Photo © Roy Anderson <habitas.org.uk>, with permission.

Figure 136. Aegopinella pura on leaf litter. Photo © Roy

Anderson <habitas.org.uk>, with permission.

Figure 137. Aegopinella nitidula on moss. Photo © Roy

Anderson <habitas.org.uk>, with permission.

Figure 138. Aegopinella nitidula showing shell coils. Photo

by Brian Eversham, with permission.

Figure 139. Clausilia bidentata on moss. Photo by


Figure 140. Clausilia rugosa on bark, a species that eats

mosses and lichens. Photo by O. Gargominy, through Creative Commons.

Eucobresia diaphana (Figure 141) lives in humid, cool places on mountains and in forests of Europe, where it is likely to encounter mosses, as seen in Figure 141 (Welter Schultes 2012b), but other than this picture, I can't verify what use it might make of them.


Figure 141. Eucobresia diaphana on a species of the moss Tortula. Photo by Stefan Haller, with permission.

On the South Pacific Kermadec Islands, Iredale (1913) remarked that in dry weather one must look for the snails among the mosses, where they hide from the dryness. He commented that they are quite variable in choice of trees, with one bole producing a dozen or more while the next half dozen adjoining trees disclose none.

Not surprisingly, new species still lurk amid the bryophytes. Efford (1998) found a new species of the carnivorous New Zealand endemic genus Rhytida (Figure 142), and reported observations by others of R. patula and R. meesoni perampla crawling on mosses and tree trunks at night. These and other New Zealand snails often fall prey to introduced predators. Wainuia urnula (Figure 143), another night-active snail on mosses, tree trunks, and rocks, was readily eaten by possums, rats, and hedgehogs in captivity. Efford (2000) found that 82% of the 315 W. urnula snails examined had an unusual food in the feces and gut – terrestrial amphipods. Its relative, W. edwardi (Figure 144), did not consume amphipods, and no other gastropod is known to consume them. The adaptation for consuming amphipods appeared to be largely behavioral, although there were some differences in the teeth.

Figure 142. Rhytida otagoensis, member of a carnivorous

genus that has some moss-dwellers. Image by James Atkinson, with permission.

Figure 143. Wainuia urnula, a tiny night-active New

Zealand endemic snail that traverses mosses, as shown here. Photo by Andrew Spurgeon, with permission.

Figure 144. Wainuia edwardi, member of a genus that lives

among mosses. Photo by James W. Atkinson, with permission.

Epiphytic

Wiesenborn (2003) observed snails in the Riverside Mountains of California and found that the active snails preferred epiphytic mosses (Figure 145) and lichens compared to plant detritus and four sizes of rocks as habitat. They suggested that the epiphytes could provide these snails with food or moisture. Tree bark soon becomes a desert after the rain dries up, but mosses remain moist much longer, permitting the snails to be active longer and to search there for food where other small invertebrates likewise take refuge from desiccation.

Figure 145. Monachoides incarnatus on bark where it often

encounters bryophytes. Photo by Stefan Haller, with permission.


Tropical islands, especially Hawaii, are particularly vulnerable to invasive species. With all the visitor traffic and import/export business, hitchhikers easily reach the islands. Snails are among these, and may be one of the causes of the apparent extinction of the bird called Po'ouli (Melamprosops phaeosoma; Figure 146) (Mountainspring et al. 1990). This native Hawaiian bird is especially adapted to feeding on land snails and insects on branches and under mosses, lichens, and bark. Its toes are large and are used for prying up moss and bark to acquire tree snails. The bill is stout, withstanding the force needed for manipulating the snails. Its demise is due largely to increased activity and habitat modification by feral pigs, avian disease, and possible gene pool impoverishment due to low numbers. But it also suffers competition for food by the introduced garlic snail (Oxychilus alliarius; Figure 147), a native of northwestern Europe (Welter Schultes 2012a) that emits a garlic odor when it is disturbed. This species is likewise a moss-dweller of mountain slope forests. It feeds on living and dead plant tissue, but it also consumes small snails and the eggs of other snails and slugs (Oxychilus 2011).

Figure 146. Poʻouli (Melamprosops phaeosoma) on a

mossy branch. Note the sturdy beak used to pry loose bark or crush snails found under bryophytes. Photo through Wikimedia Commons.

Figure 147. Oxychilus alliarius on moss on bark. Photo ©

Roy Anderson <habitas.org.uk>, with permission.

The slug Prophysaon vanattae (scarletback taildropper; Figure 148) is one of those slugs that seems to find a safe site under mosses on trees on Vancouver Island, Canada (Kristiina Ovaska, pers. comm. 30 June 2009). But it also hangs on epiphytic moss mats in the moist deciduous forest there and may even lay eggs there (Figure 149).

Pilsbry (1948) suggested that the pupillid snail Bothriopupa variolosa in eastern North America might prefer mossy rocks and trees.

Figure 148. Prophysaon vanattae, the scarletback taildropper, can be found hiding under mosses. Photo by Kristiina Ovaska, with permission.

Figure 149. Prophysaon vanattae with eggs on a moss.

Photo by Kristiina Ovaska, with permission.

Calcareous Areas

Because of the need for calcium to make the shell, many snails are dependent on limestone habitats to obtain this important resource. Hence, this is a good place to look for snails on mosses growing there.

Pupilla muscorum (Figure 150) is named for its occurrence among mosses in Great Britain, although it also occurs under stones and in leaf litter (Ehrmann 1956). This tiny (3-4 mm high shell) moss snail often prefers calciferous ground, but others describe it as indifferent to limestone content (Nordsieck 2012a). These snails are ovoviviparous. The eggs can survive over winter inside the female's body and are laid in the favorable conditions of spring. At that point, it is not the eggs that must survive because the juveniles usually hatch during oviposition. Pupilla triplicata (Figure 151) is likewise a moss dweller in Hungary and elsewhere (Deli et al. 2002).


Figure 150. Pupilla muscorum. Photo by Malcolm Storey,

through Creative Commons.

Figure 151. Pupilla triplicata, a European moss dweller.

Photo by O. Gargominy, through Creative Commons.

Another tiny conical snail (2-3 mm) of calcareous areas is Acicula fusca (Figure 152) in moss on chalk cliffs at Ballycastle, and on chalk underlying basalt at Black Head, Antrim, UK (Anderson 1996). And Pomatias elegans (Figure 153) occurs on mosses in limestone areas in the Burren, County Clare, UK (Platts et al. 2003).

Figure 152. Acicula fusca, a tiny snail that lives among

mosses on chalk cliffs. Photo © Roy Anderson <habitas.org.uk>, with permission.

Figure 153. Pomatias elegans at Cheddar, Somerset, UK.

Photo by Roger S. Key, with permission.

Trochulus (formerly Trichia) plebeia (Figure 154) occurs in wet mossy areas by springs in limestone areas (Gilbert et al. 2005). Trochulus villosus (Figure 155) lives in the German Alps and requires high moisture (Welter Schultes 2010), making bryophytes useful for maintaining that moisture. This strange genus of snails has hairs on its shell that help to hold it against wet surfaces (Gilbert et al. 2005). I don't have any indication that these hairs offer any particular help for living among bryophytes, but if they have any tactile properties, they could help keep it from getting stuck between branches by warning that the passage was getting too narrow.

Figure 154. Trochulus plebeia, a hairy snail, at Sugley

Wood, UK. Photo by Brian Eversham, with permission.

Figure 155. Trochulus villosus on mosses in Germany.

Photo by Stefan Haller, with permission.


The European family Clausiliidae, known as door snails, derive their name from the "sliding door" that covers the opening of the shell (Wikipedia 2012a). This calcareous door is known as a clausilium, hence the family name. It permits the snail to retreat into its shell and seal it off against predators. Cochlodina laminata (Figure 156), the plaited door snail, lives "between mosses" as well as leaf litter, but may also be found climbing trees in deciduous forests and montane pine forests (Welter Schultes 2012b). Clausilia dubia (Figure 157) is a calciphilic inhabitant of humid, shady rocks and old walls, but also lives on tree trunks "full of moss." Michael Proctor (pers. comm. 23 April 2016) informed me that this species is very common on Carboniferous limestone in Yorkshire Dales, UK, in the bryophyte and lichen habitats. Macrogastra ventricosa (Figure 158), the ventricose door snail, lives in places with plentiful mosses on the forest floor or on tree trunks, mostly in the mountains (Welter Schultes 2012b). Macrogastra attenuata (Figure 159) lives between moss-covered rocks as well as on stones, rocks, and leaf litter in montane forests.

Figure 156. Cochlodina laminata on bark where it appears

to be grazing mosses. Photo by Andrew Dunn, through Creative Commons.

Figure 157. Clausilia dubia with moss. Photo by O.

Gargominy, through Creative Commons.

Figure 158. Macrogastra ventricosa on moss. Photo by J.

C. Schou, Biopix, through Creative Commons.

Figure 159. Macrogastra attenuata, a species of moss-

covered rocks in montane forests of Europe. Photo by Niels Sloth, with permission.

Vertigo meramecensis (Meramac River snail), unlike a number of other members of the genus, is a strict calciphile (Nekola & Coles 2010). It is a species of special concern that lives in Iowa and Missouri, USA, and dwells in decomposed leaf litter of moss-covered ledges and shaded carbonate cliffs, among other places.

Bogs and Mires

True bogs are acid, poor fens are acid, intermediate fens have intermediate pH levels, and rich fens are basic. For a snail, that pH range is an important consideration in choice of habitat because of the need for calcium in forming a shell. Because of this relationship, most malacologists have considered Sphagnum (Figure 160) peatlands, heathlands, and pine forests as unsuitable habitats for snails and consequently have poor snail biodiversity (Karlin 1961; Kerney & Cameron 1979; Horsák & Hájek 2003).

In fact, Nekola (2010) found that highly and even moderately acidic sites had significantly (P<0.000000005) lower richness and abundance than did neutral and calcareous habitats. Nevertheless, the typical acid site supported 5-10 species.


But some snails actually thrive in the low pH of bogs and other acid habitats. One such snail is Vertigo malleata (Figure 161), an extreme calcifuge. The degree to which snails have been overlooked in these habitats is exemplified by finding this new species in 60 sites out of 100 acid sites investigated from Maine to Florida, USA (Coles & Nekola 2007). In the bogs it was found primarily in leaf litter on top of the Sphagnum (Figure 160). Nekola (Jeff Nekola, pers. comm. 16 April 2012) informed me that Vertigo malleata was virtually absent in the Sphagnum itself, occurring only where there was leaf litter on top of the Sphagnum. It would be interesting to watch its behavior if it is placed amid the Sphagnum. Is it avoiding Sphagnum, or seeking food only found among the litter? In more northern locations, V. cristata (Figure 162) or V. perryi may be present in bogs, but again, they only occur in the leaf litter, not among the Sphagnum (Jeff Nekola, pers comm. 16 April 2012). Vertigo cristata is likewise common in pine and spruce forests, heaths, and Sphagnum peatlands (Nekola & Coles 2010).

Figure 160. Sphagnum blanket bog, a habitat that does not

provide enough calcium for snails. Photo from Creative Commons.

Figure 161. Vertigo malleata from Lewis Ocean Bay, South Carolina, USA. This snail lives in Sphagnum peatlands, but avoids the Sphagnum, living in patches of leaf litter on top of it. Photo by Jeff Nekola, with permission.

Figure 162. Vertigo cristata, a species that lives on leaf

litter, but not Sphagnum, in bogs. Photo from BIO Photography Group, Biodiversity Institute of Ontario, through Creative Commons.

It appears that other snails that live in bogs and poor fens likewise typically avoid the Sphagnum (Figure 160). Like Vertigo malleata (Figure 161), Gastrocopta tappaniana occurs in decomposing leaf litter of fens, pocosins, and Sphagnum bogs (Nekola & Coles 2010). Even Vertigo perryi, a resident on the sides of Sphagnum hummocks, occurs on sedge leaf litter there. And Vertigo ventricosa (Figure 163) occurs in well-decomposed graminoid and broadleaf plant litter in the Sphagnum peatlands and poor fens.

Figure 163. Vertigo ventricosa, a species of litter in

peatlands. Photo from BIO Photography Group, Biodiversity Institute of Ontario, through Creative Commons.

Slugs have much less need for that important element – calcium (Ca). In boggy habitats, these gastropods would seem to have little choice but to travel across bryophytes (Stanisic 1996). Deroceras laeve (Figure 164) is among the slugs that traverse the complicated topography of bogs and mires. But their specific relationships to the bryophytes seems unknown. On the other hand, another


member of the genus, Deroceras reticulatum (Figure 165), is a ubiquitous slug, but Anderson (2010) points out that raised and blanket peat or exposed ground above 300 m are the only habitats where it is not likely to be found. Hence, it appears that physiological differences are important in separating these slugs.

Figure 164. Deroceras laeve (marsh slug) at Flitwick Moor,

Bedfordshire, UK. Photo by Brian Eversham, with permission.

Figure 165. Deroceras reticulatum on a bed of mosses (not Sphagnum). Photo © Roy Anderson <habitas.org.uk>, with permission.

Aquatic

In streams, it is likely that snails find mosses as a safe site from the current. Habdija et al. (2004) rarely found any gastropods on bryophytes at velocities of greater than 70 cm s-1, whereas oligochaetes became more abundant at higher velocities. Flow rates are much slower within the moss mats, thus providing a haven for feeding where the current is unlikely to dislodge the snails and slugs. This also provides them protection from predators such as fish (mostly), ducks, shore birds, and amphibians (Pennak 1953).

Frost (1942) found a strong difference in gastropod inhabitants among bryophytes between an acid and an alkaline stream in her River Liffey survey in Ireland. In the

limestone stream, she found 17 snails among the bryophytes, but she found none in the acid stream. Moss inhabitants in the limestone stream included Ancylus fluviatilis (Figure 166) and a species of Planorbis (Figure 167). She pointed out that these molluscs were only occasionally found among the mosses.

Figure 166. Ancylus fluviatilis showing its close adherence

to the substrate. Photo by Mauro Mariani, through Wikimedia Commons.

Figure 167. Planorbarius corneus. Photo © Roy Anderson


Invasive species such as the carnivorous Euglandina rosea (Figure 168), a native of tropical North America, can have severe effects on native snail species elsewhere (Kinzie 1992). In Hawaii, this species has endangered the aquatic endemic (Hawaii only) lymnaeid snails due to its seek and capture behavior. The few surviving individuals are primarily restricted to streamside seeps or damp mosses and liverworts covering rocks near waterfalls.


Figure 168. Euglandina rosea, an invasive carnivore. Photo

through Wikimedia Commons.

Plant Protectors

Not all slugs and snails seem to share a love of bryophyte habitats. As already noted, some seem to avoid them. Heinjo During has shared with me a story that unravelled in the Netherlands, published by Bart van Tooren (1990). To quote van Tooren, an increasing number of Linum (flax) seedlings correlates with an increasing number of bryophytes and other plants. Presumably, the slugs that were eating the seedlings would not traverse the bryophytes to get to these vulnerable young plants. They experimented by comparing plots with >70% cover of bryophytes with those having <20% cover. Their results were complicated by superimposing treatments of added water and/or NPK nutrients. In the control plots (no additions), the survival of Linum (flax) seedlings was greatest in plots with low bryophyte cover. However, in all three treatments at Vrakelberg the survival was greatest in plots with >70% bryophyte cover, whereas at Laamhel the addition of water plus nutrients was the only treatment that resulted in a large shift to greater survival with high bryophyte cover.

Although van Tooren (1990) was unable to demonstrate significant effects of bryophytes in his 1990 study, he and his coworkers did find them on the same slope in the 1981 study (Keizer et al. 1985). Bryophytes under the growing conditions of that year significantly reduced mortality of the tracheophytes Linum catharticum and Carlina vulgaris. Apparently, bryophytes may serve as deterrents to slugs in some years when weather conditions might otherwise encourage herbivory, but provide little support for them in years when nutrients and/or water availability are different. Such interactions between species that change with the weather require further investigation.

Mussels (Bivalve Molluscs)

Mussels are not common bryophyte inhabitants, but can occasionally occur there in aquatic environs. Frost (1942) found Sphaerium corneum (Figure 169) and four species of Pisidium (Figure 170) among the mosses in the limestone stream in her River Liffey, UK, survey, but their typical niches were elsewhere in the stream.

Some bivalve molluscs and other organisms can actually turn the relationship around and provide a home for the bryophytes. Yes, some of these animals actually have mosses growing on them. Neumann and Vidrine (1978) found Fissidens fontanus (Figure 89) and Leptodictyum riparium (Figure 171) growing on freshwater mussel shells.

Figure 169. Sphaerium corneum on an aquatic plant. Photo

© Roy Anderson <habitas.org.uk>, with permission.

Figure 170. Pisidium amnicum. Photo © Roy Anderson


Figure 171. Leptodictyum riparium, a moss known to grow on freshwater mussels. Photo by Michael Lüth, with permission.

ECHINODERMATA

I refuse to create a chapter for this marine phylum, but one observation is interesting enough to note here. Claudio Delgadillo-Moya (pers. comm. 30 March 2016) reported to me that a student who is working on sea urchins has found moss tissue in the gut of one and leafy liverwort fragments in another! There is no bryophyte known to be marine, but some do tolerate sea spray and live near the water. Most


likely one of these, no, two of these, fell into the water or washed in from a stream or river. Resourceful urchin!

Summary Snails and slugs (gastropods) have often been

observed on bryophytes. They are adapted to land with a calcified slime epiphragm to cover the shell opening and respiratory pore in the body. A radula of many teeth permits them to scrape their food. Reproduction is mostly by simultaneous hermaphroditism. This may be facilitated by a love dart that facilitates movement of sperm cells to the sperm pouch by injecting hormones. Larvae develop within the egg in most so that the gastropods are typically oviparous. A few are known to deposit eggs in mosses.

The white desert snail, Eremarionta immaculata, is common on bryophytes and seems to prefer them as a habitat. The copse snail, Arianta arbustorum is a night-active inhabitant. More quantitative studies have shown that some slugs and snails prefer bryophytes. More active snails might be found at night, whereas tiny snails might take refuge in the bryophytes during the day.

Adaptations include "jumping" (Hemphillia), small size, conical snail, hibernation/estimation, and no shell (slugs). Snails might use them as a safe site to escape spiders, daddy-long-legs, and beetles, whereas other predators may lurk among the bryophytes. In streams, bryophytes may protect them from fish, ducks, shore birds, and amphibians.

Bryophyte leafy plants and capsules can serve as food for snails and slugs, but some of these molluscs seem to avoid leaves with awns. Nutritional quality may be poor in some, and some have antiherbivore compounds that interfere with development, digestion, and palatability. In some cases the moss structure is such that the snails actually lose weight, whereas moss paste fosters a weight gain. But the gastropods may gain their nutrition from adhering algae and Cyanobacteria. In some cases protonemata and green capsules are preferred to leafy plants. Fissidens fontanus can be virtually eliminated by snails in lakes where there is no Fontinalis antipyretica to protect it. And some leafy mosses are palatable.

But some slugs won't eat the moss even when they have been starved for 7 days. They have even been observed retreating from a moss. Various phenolic compounds seem to be involved in their reluctance to eat some bryophyte species. Ricciocarpos natans has molluscicidal properties that are effective against snail vectors of schistosomiasis.

The moss may not offer any nutrition. Intact cells of leaves, capsules, and mature spores pass through the gut, and it seems that only young spores and protonemata become pale during their trip through the digestive system.

Because of their mucous trail, slugs and snails are able to disperse some bryophytes, including brood branches, spores, and leaf fragments. And it appears that the mucous helps the dispersed fragment to adhere to its new substrate. Spores can even pass through the

digestive system and survive, thus adding another form of dispersal.

Gastropods can be common among epiphytes, avoid acid habitats, and abound in limestone habitats.

Tiny mussels are able to live among bryophytes in aquatic habitats. Fissidens fontanus and Leptodictyum riparium can live on the shells.

Echinoderms generally have no association with bryophytes, but if a bryophyte falls into the marine water it may occasionally be eaten.

Acknowledgments

Bryonetters have been wonderful in making their photographs available to me and seeking photographs from others. Paul Davison has been helpful in providing suggestions and offering images. And a long time ago Allen Neumann sent me a specimen of a clam shell with Fissidens fontanus growing on it. Numerous photographers and malacologists have been helpful in providing images and information. Michael Lüth's photographs are a valued contribution. I thank all those photographers who have made their images available through the public domain.

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Documents

CHAPTER 4-8 INVERTEBRATES: MOLLUSCSInvertebrates: Molluscs. Chapt. 4-8. In: Glime, J. M. Bryophyte Ecology. Volume 2. Bryological Interaction. 4-8-1 Ebook sponsored by Michigan Technological